Technical Abstract:
Functional characterization of mycotoxin biosynthetic gene clusters has provided insights into genetic bases for variation in production of Fusarium mycotoxins. For example, production of B versus C fumonisin mycotoxins results from sequence variation in the FUM8 gene of the fumonisin biosynthetic gene (FUM) cluster. Variation in cluster sequences within and between species can also provide insight into mechanisms of evolution of clusters and mycotoxin production. Previous analyses of the Fusarium fujikuroi species complex (FFSC) revealed that phylogenetic relationships of FUM cluster sequences are not correlated with phylogenetic relationships of the producing species. Here, we conducted a battery of analyses to elucidate likely causes of this phylogenetic discord. The results indicate that: a) four phylogenetically distinct forms of the FUM cluster exist in FFSC; b) each form is located within a different genomic context; c) only one cluster form exists within a given species; and d) divergence of the FUM clusters predates divergence of the species. The results are consistent with two alternative models of evolution: a) birth-and-death evolution whereby three duplications (birth) of the entire FUM cluster in a common FFSC ancestor was followed by differential loss (death) of the resulting cluster paralogues so that extant species have no or only one cluster paralogue; and b) multiple horizontal gene transfer (HGT) events of the cluster from four relatively closely related donor species to four ancestral lineages within the FFSC. In addition, the data suggest that C-fumonisin biosynthesis evolved from B-fumonisin biosynthesis independently within two closely related FFSC lineages with different forms of the FUM cluster. The results indicate that the evolutionary history of the FUM cluster has been highly complex and provide a genetic explanation(s) for why some FFSC species produce fumonisins and contaminate crops with these mycotoxins while other species do not.